G3BP1, G3BP2 and CAPRIN1 Are Required for Translation of Interferon Stimulated mRNAs and Are Targeted by a Dengue Virus Non-coding RNA

Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human pathogens including dengue viruses (DENV). We examined three conserved host RNA-binding proteins (RBPs) G3BP1, G3BP2 and CAPRIN1 in dengue viru...

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Bibliographic Details
Published inPLoS pathogens Vol. 10; no. 7; p. e1004242
Main Authors Bidet, Katell, Dadlani, Dhivya, Garcia-Blanco, Mariano A.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.07.2014
Public Library of Science (PLoS)
Subjects
Animals
Base Sequence
Biology and Life Sciences
Carrier Proteins - genetics
Carrier Proteins - immunology
Cell Cycle Proteins - genetics
Cell Cycle Proteins - immunology
Cricetinae
Dengue
Dengue fever
Dengue Virus - immunology
DNA Helicases
eIF-2 Kinase - genetics
eIF-2 Kinase - immunology
Experiments
Gene expression
Health aspects
Humans
Immune system
Interferon
Medical research
Medical schools
Medicine and Health Sciences
Membrane Proteins - genetics
Membrane Proteins - immunology
Molecular Sequence Data
Pathogenesis
Physiological aspects
Poly-ADP-Ribose Binding Proteins
Protein Biosynthesis - immunology
Proteins
RNA
RNA Helicases
RNA Recognition Motif Proteins
RNA, Messenger - genetics
RNA, Messenger - immunology
RNA, Untranslated - genetics
RNA, Untranslated - immunology
RNA, Viral - genetics
RNA, Viral - immunology
Viral infections
Viruses
West Nile virus
Singapore
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Abstract Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human pathogens including dengue viruses (DENV). We examined three conserved host RNA-binding proteins (RBPs) G3BP1, G3BP2 and CAPRIN1 in dengue virus (DENV-2) infection and found them to be novel regulators of the interferon (IFN) response against DENV-2. The three RBPs were required for the accumulation of the protein products of several interferon stimulated genes (ISGs), and for efficient translation of PKR and IFITM2 mRNAs. This identifies G3BP1, G3BP2 and CAPRIN1 as novel regulators of the antiviral state. Their antiviral activity was antagonized by the abundant DENV-2 non-coding subgenomic flaviviral RNA (sfRNA), which bound to G3BP1, G3BP2 and CAPRIN1, inhibited their activity and lead to profound inhibition of ISG mRNA translation. This work describes a new and unexpected level of regulation for interferon stimulated gene expression and presents the first mechanism of action for an sfRNA as a molecular sponge of anti-viral effectors in human cells.
AbstractList Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human pathogens including dengue viruses (DENV). We examined three conserved host RNA-binding proteins (RBPs) G3BP1, G3BP2 and CAPRIN1 in dengue virus (DENV-2) infection and found them to be novel regulators of the interferon (IFN) response against DENV-2. The three RBPs were required for the accumulation of the protein products of several interferon stimulated genes (ISGs), and for efficient translation of PKR and IFITM2 mRNAs. This identifies G3BP1, G3BP2 and CAPRIN1 as novel regulators of the antiviral state. Their antiviral activity was antagonized by the abundant DENV-2 non-coding subgenomic flaviviral RNA (sfRNA), which bound to G3BP1, G3BP2 and CAPRIN1, inhibited their activity and lead to profound inhibition of ISG mRNA translation. This work describes a new and unexpected level of regulation for interferon stimulated gene expression and presents the first mechanism of action for an sfRNA as a molecular sponge of anti-viral effectors in human cells.Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human pathogens including dengue viruses (DENV). We examined three conserved host RNA-binding proteins (RBPs) G3BP1, G3BP2 and CAPRIN1 in dengue virus (DENV-2) infection and found them to be novel regulators of the interferon (IFN) response against DENV-2. The three RBPs were required for the accumulation of the protein products of several interferon stimulated genes (ISGs), and for efficient translation of PKR and IFITM2 mRNAs. This identifies G3BP1, G3BP2 and CAPRIN1 as novel regulators of the antiviral state. Their antiviral activity was antagonized by the abundant DENV-2 non-coding subgenomic flaviviral RNA (sfRNA), which bound to G3BP1, G3BP2 and CAPRIN1, inhibited their activity and lead to profound inhibition of ISG mRNA translation. This work describes a new and unexpected level of regulation for interferon stimulated gene expression and presents the first mechanism of action for an sfRNA as a molecular sponge of anti-viral effectors in human cells.
  Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human pathogens including dengue viruses (DENV). We examined three conserved host RNA-binding proteins (RBPs) G3BP1, G3BP2 and CAPRIN1 in dengue virus (DENV-2) infection and found them to be novel regulators of the interferon (IFN) response against DENV-2. The three RBPs were required for the accumulation of the protein products of several interferon stimulated genes (ISGs), and for efficient translation of PKR and IFITM2 mRNAs. This identifies G3BP1, G3BP2 and CAPRIN1 as novel regulators of the antiviral state. Their antiviral activity was antagonized by the abundant DENV-2 non-coding subgenomic flaviviral RNA (sfRNA), which bound to G3BP1, G3BP2 and CAPRIN1, inhibited their activity and lead to profound inhibition of ISG mRNA translation. This work describes a new and unexpected level of regulation for interferon stimulated gene expression and presents the first mechanism of action for an sfRNA as a molecular sponge of anti-viral effectors in human cells.
Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human pathogens including dengue viruses (DENV). We examined three conserved host RNA-binding proteins (RBPs) G3BP1, G3BP2 and CAPRIN1 in dengue virus (DENV-2) infection and found them to be novel regulators of the interferon (IFN) response against DENV-2. The three RBPs were required for the accumulation of the protein products of several interferon stimulated genes (ISGs), and for efficient translation of PKR and IFITM2 mRNAs. This identifies G3BP1, G3BP2 and CAPRIN1 as novel regulators of the antiviral state. Their antiviral activity was antagonized by the abundant DENV-2 non-coding subgenomic flaviviral RNA (sfRNA), which bound to G3BP1, G3BP2 and CAPRIN1, inhibited their activity and lead to profound inhibition of ISG mRNA translation. This work describes a new and unexpected level of regulation for interferon stimulated gene expression and presents the first mechanism of action for an sfRNA as a molecular sponge of anti-viral effectors in human cells.
Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human pathogens including dengue viruses (DENV). We examined three conserved host RNA-binding proteins (RBPs) G3BP1, G3BP2 and CAPRIN1 in dengue virus (DENV-2) infection and found them to be novel regulators of the interferon (IFN) response against DENV-2. The three RBPs were required for the accumulation of the protein products of several interferon stimulated genes (ISGs), and for efficient translation of PKR and IFITM2 mRNAs. This identifies G3BP1, G3BP2 and CAPRIN1 as novel regulators of the antiviral state. Their antiviral activity was antagonized by the abundant DENV-2 non-coding subgenomic flaviviral RNA (sfRNA), which bound to G3BP1, G3BP2 and CAPRIN1, inhibited their activity and lead to profound inhibition of ISG mRNA translation. This work describes a new and unexpected level of regulation for interferon stimulated gene expression and presents the first mechanism of action for an sfRNA as a molecular sponge of anti-viral effectors in human cells. Dengue virus is the most prevalent arbovirus in the world and an increasingly significant public health problem. Development of vaccines and therapeutics has been slowed by poor understanding of viral pathogenesis. Especially, how the virus subverts the host interferon response, a powerful branch of the innate immune system remains the subject of debate and great interest. Dengue virus produces large quantities of a non-coding, highly structured viral RNA, termed sfRNA, whose function in viral replication is elusive but has been linked in related viruses to inhibition of the interferon response. Nonetheless the mechanisms involved are yet to be characterized. Here, we show that dengue virus 2 sfRNA targets and antagonizes a set of host RNA-binding proteins G3BP1, G3BP2 and CAPRIN1, to interfere with translation of antiviral interferon-stimulated mRNAs. This activity impairs establishment of the antiviral state, allowing the virus to replicate and evade the interferon response. While this particular mechanism was not conserved among other flaviviruses, we believe it is highly relevant for dengue virus 2 replication and pathogenesis. Taken together, our results highlight both new layers of complexity in the regulation of the innate immune response, as well as the diversity of strategies flaviviruses employ to counteract it.
Audience Academic
Author Garcia-Blanco, Mariano A.
Bidet, Katell
Dadlani, Dhivya
AuthorAffiliation 4 Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, United States of America
Harvard Medical School, United States of America
2 NUS Graduate School for Integrative Sciences and Engineering, National University of Singapore, Singapore
3 Center for RNA Biology, Duke University Medical Center, Durham, North Carolina, United States of America
5 Department of Medicine, Duke University Medical Center, Durham, North Carolina, United States of America
1 Program in Emerging Infectious Diseases, Duke-NUS Graduate Medical School, Singapore
AuthorAffiliation_xml – name: 5 Department of Medicine, Duke University Medical Center, Durham, North Carolina, United States of America
– name: 1 Program in Emerging Infectious Diseases, Duke-NUS Graduate Medical School, Singapore
– name: 4 Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, United States of America
– name: 2 NUS Graduate School for Integrative Sciences and Engineering, National University of Singapore, Singapore
– name: 3 Center for RNA Biology, Duke University Medical Center, Durham, North Carolina, United States of America
– name: Harvard Medical School, United States of America
Author_xml – sequence: 1
  givenname: Katell
  surname: Bidet
  fullname: Bidet, Katell
– sequence: 2
  givenname: Dhivya
  surname: Dadlani
  fullname: Dadlani, Dhivya
– sequence: 3
  givenname: Mariano A.
  surname: Garcia-Blanco
  fullname: Garcia-Blanco, Mariano A.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24992036$$D View this record in MEDLINE/PubMed
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10.1128/JVI.00991-08
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Copyright COPYRIGHT 2014 Public Library of Science
2014 Bidet et al 2014 Bidet et al
2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Bidet K, Dadlani D, Garcia-Blanco MA (2014) G3BP1, G3BP2 and CAPRIN1 Are Required for Translation of Interferon Stimulated mRNAs and Are Targeted by a Dengue Virus Non-coding RNA. PLoS Pathog 10(7): e1004242. doi:10.1371/journal.ppat.1004242
Copyright_xml – notice: COPYRIGHT 2014 Public Library of Science
– notice: 2014 Bidet et al 2014 Bidet et al
– notice: 2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Bidet K, Dadlani D, Garcia-Blanco MA (2014) G3BP1, G3BP2 and CAPRIN1 Are Required for Translation of Interferon Stimulated mRNAs and Are Targeted by a Dengue Virus Non-coding RNA. PLoS Pathog 10(7): e1004242. doi:10.1371/journal.ppat.1004242
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content type line 23
Current address: SMART (Singapore-MIT Alliance for Research and Technology), Singapore
Conceived and designed the experiments: KB MAGB. Performed the experiments: KB DD. Analyzed the data: KB DD MAGB. Wrote the paper: KB MAGB.
The authors have declared that no competing interests exist.
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Snippet Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human...
  Viral RNA-host protein interactions are critical for replication of flaviviruses, a genus of positive-strand RNA viruses comprising major vector-borne human...
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StartPage e1004242
SubjectTerms Animals
Base Sequence
Biology and Life Sciences
Carrier Proteins - genetics
Carrier Proteins - immunology
Cell Cycle Proteins - genetics
Cell Cycle Proteins - immunology
Cricetinae
Dengue
Dengue fever
Dengue Virus - immunology
DNA Helicases
eIF-2 Kinase - genetics
eIF-2 Kinase - immunology
Experiments
Gene expression
Health aspects
Humans
Immune system
Interferon
Medical research
Medical schools
Medicine and Health Sciences
Membrane Proteins - genetics
Membrane Proteins - immunology
Molecular Sequence Data
Pathogenesis
Physiological aspects
Poly-ADP-Ribose Binding Proteins
Protein Biosynthesis - immunology
Proteins
RNA
RNA Helicases
RNA Recognition Motif Proteins
RNA, Messenger - genetics
RNA, Messenger - immunology
RNA, Untranslated - genetics
RNA, Untranslated - immunology
RNA, Viral - genetics
RNA, Viral - immunology
Viral infections
Viruses
West Nile virus
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Title G3BP1, G3BP2 and CAPRIN1 Are Required for Translation of Interferon Stimulated mRNAs and Are Targeted by a Dengue Virus Non-coding RNA
URI https://www.ncbi.nlm.nih.gov/pubmed/24992036
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https://pubmed.ncbi.nlm.nih.gov/PMC4081823
https://doaj.org/article/e3517f9cbf474ce48eb4c3a8dea0f2ac
http://dx.doi.org/10.1371/journal.ppat.1004242
Volume 10
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